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Phylogenetic Relationships and Biogeography of the Genus Algansea Girard (Cypriniformes: Cyprinidae) of Central Mexico Inferred from Molecular Data

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Phylogenetic Relationships and Biogeography of the Genus Algansea Girard (Cypriniformes: Cyprinidae) of Central Mexico Inferred from Molecular Data BMC Evolutionary Biology BioMed Central Research article Open Access Phylogenetic relationships and biogeography of the genus Algansea Girard (Cypriniformes: Cyprinidae) of central Mexico inferred from molecular data Rodolfo Pérez-Rodríguez*1,2, Omar Domínguez-Domínguez2, Gerardo Pérez Ponce de León3 and Ignacio Doadrio4 Address: 1Posgrado en Ciencias Biológicas, Instituto de Biología, Universidad Nacional Autónoma de México, México, D.F., México, 2Laboratorio de Biología Acuática, Facultad de Biología, Universidad Michoacana de San Nicolás de Hidalgo, Morelia, Michoacán, México, 3Instituto de Biología, Universidad Nacional Autónoma de México, Departamento de Zoología. Ap. Postal 70-153, C.P. 04510 México D.F., México and 4Departamento de Biodiversidad y Biología Evolutiva, Museo Nacional de Ciencias Naturales, CSIC, c/José Gutiérrez Abascal 2, E-28006 Madrid, España Email: Rodolfo Pérez-Rodríguez* - [email protected]; Omar Domínguez-Domínguez - [email protected]; Gerardo Pérez Ponce de León - [email protected]; Ignacio Doadrio - [email protected] * Corresponding author Published: 7 September 2009 Received: 15 January 2009 Accepted: 7 September 2009 BMC Evolutionary Biology 2009, 9:223 doi:10.1186/1471-2148-9-223 This article is available from: http://www.biomedcentral.com/1471-2148/9/223 © 2009 Pérez-Rodríguez et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Abstract Background: The genus Algansea is one of the most representative freshwater fish groups in central Mexico due to its wide geographic distribution and unusual level of endemicity. Despite the small number of species, this genus has had an unsettled taxonomic history due to high levels of intraspecific morphological variation. Moreover, several phylogenetic hypotheses among congeners have been proposed but have had the following shortcomings: the use of homoplasious morphological characters, the use of character codification and polarisation methods that lacked objectivity, and incomplete taxonomic sampling. In this study, a phylogenetic analysis among species of Algansea is presented. This analysis is based upon two molecular markers, the mitochondrial gene cytochrome b and the first intron of the ribosomal protein S7 gene. Results: Bayesian analysis based on a combined matrix (cytochrome b and first intron S7) showed that Algansea is a monophyletic group and that Agosia chrysogaster is the sister group. Divergence times dated the origin of the genus around 16.6 MYA, with subsequent cladogenetic events occurring between 6.4 and 2.8 MYA. When mapped onto the molecular phylogenetic hypothesis, the character states of three morphological characters did not support previous hypotheses on the evolution of morphological traits in the genus Algansea, whereas the character states of the remaining six characters partially corroborated those hypotheses. Conclusion: Monophyly of the genus Algansea was corroborated in this study. Tree topology shows the genus consists of three main lineages: Central-Eastern, Western, and Southern clades. However, the relationships among these clades remained unresolved. Congruence found between the available geological and climatic history and the divergence times made it possible to infer the biogeographical history of Algansea, which suggested that vicariance events were responsible for the evolutionary history of the genus. Interestingly, this pattern was shared with other members of the freshwater fish fauna of central Mexico. In addition, molecular data also show that some morphological traits alleged to represent synapomorphies in previous studies were actually homoplasies. Others traits were corroborated as synapomorphies, particularly in those species of a subgroup corresponding with the Central-Eastern clade within Algansea; this corroboration is interpreted as a result of evolutionary adaptations. Page 1 of 18 (page number not for citation purposes) BMC Evolutionary Biology 2009, 9:223 http://www.biomedcentral.com/1471-2148/9/223 Background cal characters [9,11,12,23]. Such molecular approaches Mexico lies between the Nearctic and Neotropical biogeo- demonstrated that fish diversity was in fact underesti- graphical zones and is considered to be a transitional mated because several new species were described; in zone. Because of this, it is possible to find fauna with dif- addition, some morphological characters commonly used ferent evolutionary origins [1]. One of the world's great in the classification of these groups were homoplasies. tropical-subtropical highlands is the massive uplift The genus Algansea is one of these groups that exemplify known as the Mesa Central of Mexico (MCM) and its the particular problem of using morphological characters southern limit, the Trans Mexican Volcanic Belt (TMVB). as the only source of information to establish a phyloge- Since the Miocene, this zone has experienced an active netic hypothesis. Although this genus possesses a few rep- geological history, which has promoted a complex surface resentative species, Algansea aphanea, Algansea avia, configuration, including a wide variety of ecosystems. The Algansea barbata, Algansea lacustris, Algansea monticola, freshwater fish fauna of the MCM [2,3] is unique, with Algansea popoche, Algansea tincella, [5], and Algansea ame- around 78 species, and is represented by an unusual level cae [24], its taxonomic history has been unstable, particu- of endemicity (70%) [4,5]. Most of the endemic species larly due to high levels of intraspecific morphological are represented by monophyletic groups that have under- variability found in the most widely distributed species gone a diversification process within central Mexico [6,7] within the genus, A. tincella [21]. such as the entire subfamily Goodeinae (41 species), the Atherinopsid genera Chirostoma (19 species), and three The first significant attempt to elucidate the systematic endemic genera belonging to the family Cyprinidae: relationships among species of Algansea was made by Bar- Algansea (7 species), Evarra (3 species), and Yuriria (3 spe- bour and Miller [21]. These authors studied only six valid cies) [6,8-12]. species and two subspecies and found two groups: (1) species with maxillary barbels (A. monticola - including A. Knowledge about the diversification processes of freshwa- m. monticola and A. m. avia -, A. barbata and A. aphanea) ter fish in central Mexico, including their origin as well as and (2) species without maxillary barbels (A. lacustris, A. their evolutionary and biogeographical history, is still popoche and A. tincella). In addition, based on the presence incomplete. Several hypotheses regarding the biogeogra- of a plate-like dermosphenotic bone, the genus Gila was phy of freshwater fish in the region have been discussed in determined to be the closest relative to Algansea [21]. some detail in several studies [2,3,13-17]. These authors However, current molecular studies of Mexican cyprinids described general patterns using occurrence data and mor- do not support this relationship, and these analyses estab- phological comparisons. More recently, studies that incor- lished the genus Agosia as the sister group of Algansea porated molecular approaches in a phylogenetic context [10,12]. Subsequent to Barbour and Miller's hypothesis, have been conducted to elucidate the biogeographical and the subspecies A. m. avia was validated as an independent evolutionary history of fish in central Mexico among species, A. avia. This species, together with A. monticola, A. groups such as poecilids [18], goodeids [7,9,19], and barbata, and A. aphanea, are the barbeled species. The last cyprinids [10,12]. All of these studies agree that the histor- taxonomic change implied that the highly differentiated ical biogeography of central Mexico and its freshwater fish population of A. tincella from the Ameca River should be fauna is linked to the intense geological activity since the recognised as A. amecae [24]. All the aforementioned sug- early Miocene. This activity has generated a complex gest that the morphological characters on which those hydrological system characterised by high dynamism and first analyses were based have evolved independently sev- the formation and destruction of drainages. This dyna- eral times throughout the evolutionary history of mism promoted vicariance, taxon-pulse, and species- cyprinids [25], resulting in controversial classification pulse events [20]. However, the complexity of these bio- schemes [26]. geographic patterns and the few fish groups studied thus far make it necessary to study other co-distributed fish Molecular markers have proven to be very useful tools groups, such as members of the genus Algansea, to formu- when elucidating the phylogenetic relationships of verte- late a more robust biogeographical scenario of the area. brate groups. In the last few years, the mitochondrial gene cytochrome b (cyt b) and the first intron of the S7 ribos- The first attempts to uncover phylogenetic patterns of omal protein gene have been used in different phyloge- freshwater fish in central Mexico were based on just a few netic analyses to provide insights into the fish morphological traits, resulting in a non-robust hypothesis evolutionary history at various taxonomic levels. Both regarding
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